BCR/ABL translocates to the nucleus and disrupts an ATR-dependent intra-S phase checkpoint
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Chronic myelogeneous leukemia (CML) is a two-stage disease associated with expression of the BCR/ABL tyrosine kinase protein. However, whether BCR/ABL expression directly causes blast crisis, and if so by what mechanism, is unknown. We have found that BCR/ABL translocates from the cytoplasm to the nucleus after genotoxic stress. Furthermore, BCR/ABL increases DNA double-strand damage after etoposide treatment and leads to a defect in an intra-S phase checkpoint, causing a radioresistant DNA synthesis (RDS) phenotype. In the nucleus, BCR/ABL associates with the ataxia-telangiectasia and rad 3-related protein (ATR) and disrupts ATR-dependent signal transduction. Overexpression of ATR in a BCR/ABL-expressing cell line corrects the DNA damage phenotype. These results demonstrate a nuclear role for BCR/ABL in altering the cellular response to DNA damage.
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BCR-ABL disrupts ATR-dependent intra-S phase checkpoint in chronic myeloid leukemia after etoposide treatment, by causing DNA strand break formation.
“The oncogenic BCR-ABL fusion protein disrupts ATR-dependent intra-S phase checkpoint in chronic myeloid leukemia after etoposide treatment, by causing DNA strand break formation [33].”
From The Spi1/PU.1 transcription factor accelerates replication fork progression by increasing PP1 phosphatase in leukemia (2017) · cites this paper as [33]
Cites
A simple technique for quantitation of low levels of DNA damage in individual cells
Singh, N. P., McCoy, M. T., Tice, R. R., & Schneider, E. L. (1988) · Experimental Cell Research · doi:10.1016/0014-4827(88)90265-0 · Cited by 10,828 · see citing works
Druker, B. J., Talpaz, M., Resta, D. J., Peng, B., Buchdunger, E., Ford, J., Lydon, N., Kantarjian, H. M., Capdeville, R., Ohno-Jones, S., et al. (2001) · New England Journal of Medicine · doi:10.1056/nejm200104053441401 · Cited by 5,237 · see citing works
Daley, G. Q., Etten, R. A. V., & Baltimore, D. (1990) · Science · doi:10.1126/science.2406902 · Cited by 2,141 · see citing works
Cell cycle checkpoint signaling through the ATM and ATR kinases
Abraham, R. T. (2001) · Genes & Development · doi:10.1101/gad.914401 · Cited by 1,966 · see citing works
Liu, Q., Guntuku, S., Cui, X.-S., Matsuoka, S., Cortez, D., Tamai, K., Luo, G., Carattini-Rivera, S., DeMayo, F., Bradley, A., et al. (2000) · Genes & Development · doi:10.1101/gad.14.12.1448 · Cited by 1,625 · see citing works
<i>ATR</i> disruption leads to chromosomal fragmentation and early embryonic lethality
Brown, E. J., & Baltimore, D. (2000) · Genes & Development · doi:10.1101/gad.14.4.397 · Cited by 951 · see citing works
The tyrosine kinase c-Abl regulates p73 in apoptotic response to cisplatin-induced DNA damage
Gong, J., Costanzo, A., Yang, H., Melino, G., Kaelin, W. G., Levrero, M., & Wang, J. Y. J. (1999) · Nature · doi:10.1038/21690 · Cited by 923 · see citing works
Konopka, J. B., Watanabe, S. M., & Witte, O. N. (1984) · Cell · doi:10.1016/0092-8674(84)90438-0 · Cited by 872 · see citing works
Radiosensitivity in ataxia-telangiectasia: a new explanation.
Painter, R. B., & Young, B. R. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.12.7315 · Cited by 794 · see citing works
Pear, W. S., Miller, J. P., Xu, L., Pui, J. C., Soffer, B., Quackenbush, R. C., Pendergast, A. M., Bronson, R. T., Aster, J. C., Scott, M. L., et al. (1998) · Blood · doi:10.1182/blood.v92.10.3780 · Cited by 755 · see citing works
Sørensen, C. S., Syljuåsen, R. G., Falck, J., Schroeder, T., Rönnstrand, L., Khanna, K. K., Zhou, B.-B., Bártek, J., & Lukas, J. (2003) · Cancer Cell · doi:10.1016/s1535-6108(03)00048-5 · Cited by 560 · see citing works
Interaction of c-Abl and p73α and their collaboration to induce apoptosis
Agami, R., Blandino, G., Oren, M., & Shaul, Y. (1999) · Nature · doi:10.1038/21697 · Cited by 544 · see citing works
Baskaran, R., Wood, L. D., Whitaker, L. L., Canman, C. E., Morgan, S. E., Xu, Y., Barlow, C., Baltimore, D., Wynshaw-Boris, A. J., Kastan, M. B., et al. (1997) · Nature · doi:10.1038/387516a0 · Cited by 538 · see citing works
Cliby, W. A., Roberts, C. J., Cimprich, K. A., Stringer, C. M., Lamb, J. R., Schreiber, S. L., & Friend, S. H. (1998) · The EMBO Journal · doi:10.1093/emboj/17.1.159 · Cited by 534 · see citing works
Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance
Brown, E. J., & Baltimore, D. (2003) · Genes & Development · doi:10.1101/gad.1067403 · Cited by 511 · see citing works
Inhibition of apoptosis by BCR-ABL in chronic myeloid leukemia
Bedi, A., Zehnbauer, B., Barber, J. P., Sharkis, S. J., & Jones, R. (1994) · Blood · doi:10.1182/blood.v83.8.2038.2038 · Cited by 506 · see citing works
Interaction between ATM protein and c-Abl in response to DNA damage
Shafman, T. D., Khanna, K. K., Kedar, P. S., Spring, K. J., Kozlov, S., Yen, T. J., Hobson, K., Gatei, M. H., Zhang, N., Watters, D. J., et al. (1997) · Nature · doi:10.1038/387520a0 · Cited by 478 · see citing works
Maintenance of Genome Stability in Saccharomyces cerevisiae
Kolodner, R. D., Putnam, C. D., & Myung, K. (2002) · Science · doi:10.1126/science.1075277 · Cited by 464 · see citing works
Etten, R. A. V., Jackson, P. K., & Baltimore, D. (1989) · Cell · doi:10.1016/0092-8674(89)90102-5 · Cited by 425 · see citing works
An ATR- and Cdc7-Dependent DNA Damage Checkpoint that Inhibits Initiation of DNA Replication
Costanzo, V., Shechter, D., Lupardus, P. J., Cimprich, K. A., Gottesman, M. E., & Gautier, J. (2003) · Molecular Cell · doi:10.1016/s1097-2765(02)00799-2 · Cited by 355 · see citing works
Vigneri, P. G., & Wang, J. Y. J. (2001) · Nature Medicine · doi:10.1038/84683 · Cited by 333 · see citing works
BCR/ABL Regulates Mammalian RecA Homologs, Resulting in Drug Resistance
Słupianek, A., Schmütte, C., Tombline, G., Nieborowska-Skorska, M., Hoser, G., Nowicki, M. O., Pierce, A. J., Fishel, R. A., & Skórski, T. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00357-4 · Cited by 313 · see citing works
Nuclear-cytoplasmic shuttling of C-ABL tyrosine kinase
Taagepera, S., McDonald, D., Loeb, J. E., Whitaker, L. L., McElroy, A. K., Wang, J. Y. J., & Hope, T. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.13.7457 · Cited by 311 · see citing works
Ahuja, H., Bar‐Eli, M., Advani, S. H., Benchimol, S., & Cline, M. J. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.17.6783 · Cited by 284 · see citing works
Regulation of cell death by the Abl tyrosine kinase
Wang, J. Y. J. (2000) · Oncogene · doi:10.1038/sj.onc.1203878 · Cited by 278 · see citing works
Ye, X., Franco, A. A., Santos, H., Nelson, D. M., Kaufman, P. D., & Adams, P. D. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00037-6 · Cited by 262 · see citing works
Heffernan, T. P., Simpson, D. A., Frank, A. R., Heinloth, A. N., Paules, R. S., Cordeiro-Stone, M., & Kaufmann, W. K. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.24.8552-8561.2002 · Cited by 251 · see citing works
Radiosensitivity in ataxia-telangiectasia
Cunliffe, P. N., Mann, J. R., Cameron, A., Roberts, K. D., & Ward, H. W. C. (1975) · British Journal of Radiology · doi:10.1259/0007-1285-48-569-374 · Cited by 189 · see citing works
Wetzler, M., Talpaz, M., Etten, R. A. V., Hirsch‐Ginsberg, C., Beran, M., & Kurzrock, R. (1993) · Journal of Clinical Investigation · doi:10.1172/jci116786 · Cited by 188 · see citing works
Neshat, M. S., Raitano, A. B., Wang, H., Reed, J. C., & Sawyers, C. L. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.4.1179-1186.2000 · Cited by 185 · see citing works
Determination of cell fate by c-Abl activation in the response to DNA damage
Kharbanda, S. M., Yuan, Z.-M., Weichselbaum, R. W., & Kufe, D. W. (1998) · Oncogene · doi:10.1038/sj.onc.1202571 · Cited by 166 · see citing works
BCR-ABL down-regulates the DNA repair protein DNA-PKcs
Deutsch, É., Dugray, A., Abdulkarim, B., Marangoni, E., Maggiorella, L., Vaganay, S., M'Kacher, R., Douc‐Rasy, S., Eschwège, F., Vainchenker, W., et al. (2001) · Blood · doi:10.1182/blood.v97.7.2084 · Cited by 166 · see citing works
Initiation of Deregulated Growth of Multipotent Progenitor Cells by bcr-abl in Vitro
Gishizky, M. L., & Witte, O. N. (1992) · Science · doi:10.1126/science.1375394 · Cited by 160 · see citing works
Salesse, S., & Verfaillie, C. M. (2002) · Oncogene · doi:10.1038/sj.onc.1206082 · Cited by 137 · see citing works
Secondary mutation maintains the transformed state in BaF3 cells with inducible BCR/ABL expression.
Klucher, K., Lopez, D. V., & Daley, G. (1998) · Blood · doi:10.1182/blood.v91.10.3927.3927_3927_3934 · Cited by 133 · see citing works
Secondary Mutation Maintains the Transformed State in BaF3 Cells With Inducible BCR/ABL Expression
Klucher, K. M., Lopez, D. V., & Daley, G. Q. (1998) · Blood · doi:10.1182/blood.v91.10.3927 · Cited by 122 · see citing works
Down-regulation of BRCA1 in BCR-ABL–expressing hematopoietic cells
Deutsch, É., Jarrousse, S., Selimoglu‐Buet, D., Dugray, A., Bonnet, M., Vozenin, M., Guilhot, F., Turhan, A. G., Feunteun, J., & Bourhis, J. (2003) · Blood · doi:10.1182/blood-2002-10-3011 · Cited by 100 · see citing works
The BCR-ABL oncoprotein potentially interacts with the xeroderma pigmentosum group B protein
Takeda, N., Shibuya, M., & Maru, Y. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.1.203 · Cited by 79 · see citing works
White, E., & Prives, C. L. (1999) · Nature · doi:10.1038/21539 · Cited by 65 · see citing works
Majsterek, I., Błasiak, J., Mlynarski, W. M., Hoser, G., & Skórski, T. (2002) · Cell Biology International · doi:10.1006/cbir.2002.0865 · Cited by 33 · see citing works
Karyotype abnormalities and their clinical significance in blast crisis of chronic myeloid leukemia
Grießhammer, M., Heinze, B., Bangerter, M., Heimpel, H., & Fliedner, T. M. (1997) · Journal of Molecular Medicine · doi:10.1007/s001090050173 · Cited by 30 · see citing works
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Checking on DNA damage in S phase
Bartek, J., Lukas, C., & Lukas, J. (2004) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1493 · Cited by 758 · see citing works
Chronic myeloid leukaemia as a model of disease evolution in human cancer
Melo, J. V., & Barnes, D. J. (2007) · Nature reviews. Cancer · doi:10.1038/nrc2147 · Cited by 616 · see citing works
The biology of CML blast crisis
Calabretta, B., & Perrotti, D. (2004) · Blood · doi:10.1182/blood-2003-12-4111 · Cited by 591 · see citing works
Cell Cycle Regulation of DNA Replication
Sclafani, R. A., & Holzen, T. M. (2007) · Annual Review of Genetics · doi:10.1146/annurev.genet.41.110306.130308 · Cited by 448 · see citing works
Willis, S. G., Lange, T., Demehri, S., Otto, S., Crossman, L. C., Niederwieser, D. W., Stoffregen, E. P., McWeeney, S. K., Kovacs, I., Park, B. S., et al. (2005) · Blood · doi:10.1182/blood-2005-03-1036 · Cited by 298 · see citing works
Nowicki, M. O., Falinski, R., Koptyra, M., Słupianek, A., Stokłosa, T., Gloc, E., Nieborowska-Skorska, M., Błasiak, J., & Skórski, T. (2004) · Blood · doi:10.1182/blood-2004-05-1941 · Cited by 271 · see citing works
Cellular response to etoposide treatment
Montecucco, A., & Biamonti, G. (2006) · Cancer Letters · doi:10.1016/j.canlet.2006.11.005 · Cited by 231 · see citing works
Gain-of-function mutation of GATA-2 in acute myeloid transformation of chronic myeloid leukemia
Zhang, S., Ma, L., Huang, Q., Guo, L., Gu, B.-W., Gao, X., Shi, J.-Y., Wang, Y., Gao, L., Cai, X., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711824105 · Cited by 181 · see citing works
Applying the discovery of the Philadelphia chromosome
Sherbenou, D. W., & Druker, B. J. (2007) · Journal of Clinical Investigation · doi:10.1172/jci31988 · Cited by 119 · see citing works
BCR–ABL: a multi-faceted promoter of DNA mutation in chronic myelogeneous leukemia
Burke, B. A., & Carroll, M. P. (2010) · Leukemia · doi:10.1038/leu.2010.67 · Cited by 89 · see citing works
Self-citationStructural Basis for the Cytoskeletal Association of Bcr-Abl/c-Abl
Hantschel, O. D., Wiesner, S., Guettler, T., Mackereth, C. D., Rix, L. L. R., Mikes, Z., Dehne, J., Görlich, D., Sattler, M., & Superti‐Furga, G. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.06.030 · Cited by 81 · see citing works
Cdc7 Is an Active Kinase in Human Cancer Cells Undergoing Replication Stress
Tenca, P., Brotherton, D. H., Montagnoli, A., Rainoldi, S., Albanese, C., & Santocanale, C. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m604457200 · Cited by 81 · see citing works
Yamada, M., Watanabe, K., Mistrík, M., Veselá, E., Protivankova, I., Mailand, N., Lee, M., Masai, H., Lukas, J., & Bartek, J. (2013) · Genes & Development · doi:10.1101/gad.224568.113 · Cited by 81 · see citing works
Cdc7 kinase – A new target for drug development
Swords, R. T., Mahalingam, D., O'Dwyer, M. E., Santocanale, C., Kelly, K. R., Carew, J. S., & Giles, F. J. (2009) · European Journal of Cancer · doi:10.1016/j.ejca.2009.09.020 · Cited by 79 · see citing works
Cdc7-Dbf4 and the Human S Checkpoint Response to UVC
Heffernan, T. P., Ünsal-Kaçmaz, K., Heinloth, A. N., Simpson, D. A., Paules, R. S., Sancar, A., Cordeiro‐Stone, M., & Kaufmann, W. K. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m611292200 · Cited by 78 · see citing works
BCR/ABL modifies the kinetics and fidelity of DNA double-strand breaks repair in hematopoietic cells
Słupianek, A., Nowicki, M. O., Koptyra, M., & Skórski, T. (2005) · DNA repair · doi:10.1016/j.dnarep.2005.10.005 · Cited by 75 · see citing works
Fusion tyrosine kinases: a result and cause of genomic instability
Penserga, E. T. P., & Skórski, T. (2006) · Oncogene · doi:10.1038/sj.onc.1209756 · Cited by 75 · see citing works
Nuclear trafficking of pro-apoptotic kinases in response to DNA damage
Yoshida, K. (2008) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2008.05.003 · Cited by 74 · see citing works
Cellular and Clinical Impact of Haploinsufficiency for Genes Involved in ATR Signaling
O’Driscoll, M., Dobyns, W. B., van Hagen, J. M., & Jeggo, P. A. (2007) · The American Journal of Human Genetics · doi:10.1086/518696 · Cited by 73 · see citing works
Signaling Networks Associated with BCR–ABL–Dependent Transformation
Hazlehurst, L., Bewry, N. N., Nair, R. R., & Pinilla-Ibarz, J. A. (2009) · Cancer Control · doi:10.1177/107327480901600202 · Cited by 69 · see citing works
The Role of Dbf4/Drf1-Dependent Kinase Cdc7 in DNA-Damage Checkpoint Control
Tsuji, T., Lau, E. K., Chiang, G. G., & Jiang, W. B. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.12.005 · Cited by 62 · see citing works
ATR-Chk1 Axis Protects BCR/ABL Leukemia Cells from the Lethal Effect of DNA Double-Strand Breaks
Nieborowska-Skorska, M., Stokłosa, T., Datta, M., Czechowska, A., Rink, L. A., Słupianek, A., Koptyra, M., Seferyńska, I., Krszyna, K., Błasiak, J., et al. (2006) · Cell Cycle · doi:10.4161/cc.5.9.2722 · Cited by 59 · see citing works
Nihira, K., Taira, N., Miki, Y., & Yoshida, K. (2008) · Oncogene · doi:10.1038/onc.2008.334 · Cited by 58 · see citing works
BCR-ABL promotes the frequency of mutagenic single-strand annealing DNA repair
Fernandes, M. S., Reddy, M. M., Gonneville, J. R., DeRoo, S. C., Podar, K., Griffin, J. D., Weinstock, D. M., & Sattler, M. (2009) · Blood · doi:10.1182/blood-2008-07-172148 · Cited by 58 · see citing works
Rodrigues, M. S., Reddy, M. M., & Sattler, M. (2008) · Antioxidants and Redox Signaling · doi:10.1089/ars.2008.2071 · Cited by 57 · see citing works
The human intra-S checkpoint response to UVC-induced DNA damage
Kaufmann, W. K. (2009) · Carcinogenesis · doi:10.1093/carcin/bgp230 · Cited by 52 · see citing works
Lee, A. Y., Chiba, T., Truong, L. N., Cheng, A. N., Do, J. P. H., Cho, M. J., Chen, L., & Wu, X. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.291104 · Cited by 52 · see citing works
Regulation of the initiation of DNA replication in human cells
Moiseeva, T. N., & Bakkenist, C. J. (2018) · DNA repair · doi:10.1016/j.dnarep.2018.09.003 · Cited by 51 · see citing works
Molecular Pathogenesis of MLL-Associated Leukemias
Eguchi, M., Eguchi‐Ishimae, M., & Greaves, M. F. (2005) · International Journal of Hematology · doi:10.1532/ijh97.05042 · Cited by 50 · see citing works
Molecular architecture of the DNA replication origin activation checkpoint
Tudzarova, S., Trotter, M. W. B., Wollenschlaeger, A., Mulvey, C. M., Godovac‐Zimmermann, J., Williams, G. H., & Stoeber, K. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.201 · Cited by 49 · see citing works
Regulation and roles of Cdc7 kinase under replication stress
Yamada, M., Masai, H., & Bártek, J. (2014) · Cell Cycle · doi:10.4161/cc.29251 · Cited by 41 · see citing works
Pathobiology of Lymphoid and Myeloid Blast Crisis and Management Issues
Ilaria, R. L. (2005) · Hematology · doi:10.1182/asheducation-2005.1.188 · Cited by 41 · see citing works
Chakraborty, S., Stark, J. M., Sun, C., Modi, H., Chen, W., O'Connor, T. R., Forman, S. J., Bhatia, S., & Bhatia, R. (2012) · Blood · doi:10.1182/blood-2011-05-352252 · Cited by 40 · see citing works
Mouse models for ATR deficiency
O’Driscoll, M. (2009) · DNA repair · doi:10.1016/j.dnarep.2009.09.001 · Cited by 40 · see citing works
ATR-CHK1 pathway as a therapeutic target for acute and chronic leukemias
Boudný, M., & Trbušek, M. (2020) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2020.102026 · Cited by 40 · see citing works
Genetic Biomarkers in Chronic Myeloid Leukemia: What Have We Learned So Far?
Abdulmawjood, B., Costa, B. G. L. D. M., Roma‐Rodrigues, C., Baptista, P. V., & Fernandes, A. R. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222212516 · Cited by 36 · see citing works
Kinase-Independent Mechanisms of Resistance of Leukemia Stem Cells to Tyrosine Kinase Inhibitors
Ichim, C. V. (2014) · Stem Cells Translational Medicine · doi:10.5966/sctm.2012-0159 · Cited by 35 · see citing works
Poh, W. T., Chadha, G. S., Gillespie, P. J., Kaldis, P., & Blow, J. J. (2014) · Open Biology · doi:10.1098/rsob.130138 · Cited by 35 · see citing works
14‐3‐3 Ligand Prevents Nuclear Import of c‐ABL Protein in Chronic Myeloid Leukemia
Mancini, M., Veljković, N., Corradi, V., Zuffa, E., Corrado, P., Pagnotta, E., Martinelli, G., Barbieri, E., & Santucci, M. A. (2009) · Traffic · doi:10.1111/j.1600-0854.2009.00897.x · Cited by 34 · see citing works
Drug design with Cdc7 kinase: a potential novel cancer therapy target
Masai, H. (2008) · Drug Design Development and Therapy · doi:10.2147/dddt.s4303 · Cited by 34 · see citing works
BCR/ABL induces chromosomal instability after genotoxic stress and alters the cell death threshold
Dierov, J. K., Sanchez, P. V., Burke, B. A., Padilla‐Nash, H. M., Putt, M. E., Ried, T., & Carroll, M. P. (2008) · Leukemia · doi:10.1038/leu.2008.308 · Cited by 33 · see citing works
Self-citationLi, S., & Li, D. (2007) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2007.00108.x · Cited by 33 · see citing works
Rink, L. A., Słupianek, A., Stokłosa, T., Nieborowska-Skorska, M., Urbańska, K., Seferyńska, I., Krzysztof Reiss, F., & Skórski, T. (2007) · Blood · doi:10.1182/blood-2006-08-042630 · Cited by 32 · see citing works
BRIT1/MCPH1 Expression in Chronic Myeloid Leukemia and Its Regulation of the G2/M Checkpoint
Giallongo, C., Tibullo, D., Cava, P. L., Branca, A., Parrinello, N. L., Spina, P., Stagno, F., Conticello, C., Chiarenza, A., Vigneri, P. G., et al. (2011) · Acta Haematologica · doi:10.1159/000329911 · Cited by 31 · see citing works
Genomic instability: The cause and effect of BCR/ABL tyrosine kinase
Skórski, T. (2007) · Current Hematologic Malignancy Reports · doi:10.1007/s11899-007-0010-6 · Cited by 31 · see citing works
Fusion tyrosine kinase mediated signalling pathways in the transformation of haematopoietic cells
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Dohrmann, P. R., & Sclafani, R. A. (2006) · Genetics · doi:10.1534/genetics.106.060236 · Cited by 30 · see citing works
Lange, T., Park, B. S., Willis, S. G., & Deininger, M. W. (2005) · Cell Cycle · doi:10.4161/cc.4.12.2261 · Cited by 30 · see citing works
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Kwok, M., Agathanggelou, A., & Stanković, T. (2024) · Blood · doi:10.1182/blood.2023019963 · Cited by 28 · see citing works
Graphene quantum dots decorated with imatinib for leukemia treatment
Félix, D. M., Alencar, L. M. R., de Menezes, F. D., Midlej, V. D. V. P., Aguiar, L., Piperni, S. G., Zhang, J., Liu, Y., Ricci‐Júnior, E., Alexis, F., et al. (2020) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2020.102117 · Cited by 28 · see citing works
Wei, F., Yan, J., Tang, D., Lin, X., He, L., Xie, Y., Tao, L., & Wang, S. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2012.10.016 · Cited by 28 · see citing works
Inhibition of the NADPH oxidase regulates heme oxygenase 1 expression in chronic myeloid leukemia
Singh, M. M., Irwin, M. E., Gao, Y. H., Ban, K., Shi, P., Arlinghaus, R. B., Amin, H. M., & Chandra, J. (2011) · Cancer · doi:10.1002/cncr.26621 · Cited by 27 · see citing works
Genomic Instability in Chronic Myeloid Leukemia: Targets for Therapy?
Muvarak, N. E., Nagaria, P. K., & Rassool, F. V. (2012) · Current Hematologic Malignancy Reports · doi:10.1007/s11899-012-0119-0 · Cited by 26 · see citing works
BLM helicase is activated in BCR/ABL leukemia cells to modulate responses to cisplatin
Słupianek, A., Gurdek, E., Koptyra, M., Nowicki, M. O., Siddiqui, K. M., Groden, J. L., & Skórski, T. (2005) · Oncogene · doi:10.1038/sj.onc.1208545 · Cited by 26 · see citing works
Sasi, N. K., Coquel, F., Lin, Y., MacKeigan, J. P., Pasero, P., & Weinreich, M. (2018) · Neoplasia · doi:10.1016/j.neo.2018.08.001 · Cited by 25 · see citing works
Chronic myeloid leukemia: why does it evolve from chronic phase to blast transformation?
Tariq, I. (2006) · Frontiers in bioscience · doi:10.2741/1791 · Cited by 25 · see citing works
Skorta, I., Oren, M., Markwardt, C., Gutekunst, M., Aulitzky, W. E., & van der Kuip, H. (2009) · Cancer Research · doi:10.1158/0008-5472.can-09-0548 · Cited by 24 · see citing works
Stress and death: breaking up the c-Abl/14-3-3 complex in apoptosis
Pendergast, A. M. (2005) · Nature Cell Biology · doi:10.1038/ncb0305-213 · Cited by 24 · see citing works
Regulation for Nuclear Targeting of the Abl Tyrosine Kinase in Response to DNA Damage
Yoshida, K. (2007) · Advances in experimental medicine and biology · doi:10.1007/978-0-387-69116-9_15 · Cited by 23 · see citing works
The DNA damage response during an unperturbed S-phase
Ben‐Yehoyada, M., Gautier, J., & Dupré, A. (2007) · DNA repair · doi:10.1016/j.dnarep.2007.02.005 · Cited by 23 · see citing works
Xu, T., Gu, J., Zhou, Y., & Du, L. (2009) · BMC Bioinformatics · doi:10.1186/1471-2105-10-240 · Cited by 21 · see citing works
Stetka, J., Gurský, J., Velasquez, J. L., Mojzíková, R., Vyhlidalova, P., Vráblová, L., Bártek, J., & Divoký, V. (2020) · Cancers · doi:10.3390/cancers12040903 · Cited by 19 · see citing works
Loss of CCDC6 Affects Cell Cycle through Impaired Intra-S-Phase Checkpoint Control
Thanasopoulou, A., Stravopodis, D. J., DIMAS, K. S., Schwaller, J., & Anastasiadou, E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031007 · Cited by 19 · see citing works
Inhibition of DNA Damage-induced Apoptosis through Cdc7-mediated Stabilization of Tob
Suzuki, T., Kawamura-Tsuzuku, J., Hayashi, A., Shiomi, Y., Iwanari, H., Mochizuki, Y., Hamakubo, T., Kodama, T., Nishitani, H., Masai, H., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.353805 · Cited by 18 · see citing works
Chk1 inhibitors overcome imatinib resistance in chronic myeloid leukemia cells
Lei, H., Jin, J., Liu, M., Li, X., Luo, H., Li, Y., Xu, H., & Wu, Y. (2017) · Leukemia Research · doi:10.1016/j.leukres.2017.11.007 · Cited by 17 · see citing works
Identification of TopBP1 as a c-Abl-interacting Protein and a Repressor for c-Abl Expression
Zeng, L., Hu, Y., & Li, B. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m503016200 · Cited by 17 · see citing works
Jusoh, S. A. M., Al‐Jamal, H. A. N., Ang, C. Y., Asan, J. M., Seeni, A., & Johan, M. F. (2014) · Asian Pacific Journal of Cancer Prevention · doi:10.7314/apjcp.2014.15.1.475 · Cited by 16 · see citing works
Sengupta, A., Banerjee, D., Chandra, S., & Banerjee, S. (2006) · The Journal of Gene Medicine · doi:10.1002/jgm.959 · Cited by 16 · see citing works
Deręgowska, A., Pępek, M., Pruszczyk, K., Machnicki, M. M., Wnuk, M., & Stokłosa, T. (2020) · Genes · doi:10.3390/genes11101145 · Cited by 13 · see citing works
Martin, M. G., DiPersio, J. F., & Uy, G. L. (2009) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.1080/10428190802517765 · Cited by 12 · see citing works
Rimmelé, P., Esposito, M., Delestré, L., Guervilly, J.-H., Ridinger-Saison, M., Despras, E., Moreau-Gachelin, F., Rosselli, F., & Guillouf, C. (2017) · Oncotarget · doi:10.18632/oncotarget.16183 · Cited by 11 · see citing works
“The oncogenic BCR-ABL fusion protein disrupts ATRdependent intra-S phase checkpoint in chronic myeloid leukemia after etoposide treatment, by causing DNA strand break formation [33].”
BackgroundChromosomal Instability in Chronic Myeloid Leukemia: Mechanistic Insights and Effects
Senapati, J., & Sasaki, K. (2022) · Cancers · doi:10.3390/cancers14102533 · Cited by 11 · see citing works
Kim, Y.-M., Lee, Y. M., Park, S., & Pyo, H. (2011) · DNA and Cell Biology · doi:10.1089/dna.2010.1141 · Cited by 10 · see citing works
Zamani, A., Jusoh, S. A. M., Al‐Jamal, H. A. N., Sul’ain, M. D., & Johan, M. F. (2016) · Europe PMC (PubMed Central) · doi:10.22034/apjcp.2016.17.11.4857 · Cited by 8 · see citing works
Huguet, F., Giocanti, N., Hennequin, C., Croisy‐Delcey, M., Touboul, E., & Favaudon, V. (2008) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-07-2023 · Cited by 8 · see citing works
Src kinases as targets for Bcell acute lymphoblastic leukaemia therapy
Li, S. (2005) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.9.2.329 · Cited by 8 · see citing works
REXO5 promotes genomic integrity through regulating R-loop using its exonuclease activity
Lee, Y. J., Lee, S. Y., Kim, S.-M., Kim, S.-H., Lee, S. H., Park, S., Kim, J. J., Kim, D., & Kim, H. (2024) · Leukemia · doi:10.1038/s41375-024-02362-z · Cited by 7 · see citing works
Tumor Suppressor Genes in Myeloid Differentiation and Leukemogenesis
Britschgi, C., & Fey, M. F. (2009) · Future Oncology · doi:10.2217/14796694.5.2.245 · Cited by 7 · see citing works
Role of the C‐terminal actin binding domain in BCR/ABL‐mediated survival and drug resistance
Underhill-Day, N., Pierce, A., Thompson, S., Xenaki, D., Whetton, A. D., & Owen‐Lynch, P. J. (2006) · British Journal of Haematology · doi:10.1111/j.1365-2141.2005.05949.x · Cited by 7 · see citing works
Kundu, M., Dey, A., & Dasgupta, S. (2025) · Current Problems in Cancer · doi:10.1016/j.currproblcancer.2025.101206 · Cited by 6 · see citing works
Mouse Models of Human Blood Cancers
Li, S. (2008) · Springer eBooks · doi:10.1007/978-0-387-69132-9 · Cited by 6 · see citing works
Targeting cell cycle checkpoints for glioma therapy
Lang, F., & Yang, C. (2025) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2025.108932 · Cited by 4 · see citing works
Chronic Myeloid Leukemia: Biology of Advanced Phase
Melo, J. V., & Barnes, D. (2007) · Springer eBooks · doi:10.1007/978-3-540-34506-0_3 · Cited by 4 · see citing works
Zhang, X., Jia, D., Ao, J., Liu, H., Zang, Y., Azam, M., Habib, S. L., Li, J., Ruan, X., Jia, H., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.11566 · Cited by 4 · see citing works
Fukumoto, Y., Hoshino, T., Nakayama, Y., & Ogra, Y. (2023) · DNA repair · doi:10.1016/j.dnarep.2023.103567 · Cited by 3 · see citing works
Pannucci, N. L., Li, D., Sahay, S., Thomas, E. K., Chen, R., Tala, I., Hu, T., Ciccarelli, B. T., Megjugorac, N. J., Adams, H., et al. (2013) · Blood Cancer Journal · doi:10.1038/bcj.2013.36 · Cited by 3 · see citing works
(2017) · Cancer Studies and Therapeutics · doi:10.31038/cst.2017232 · Cited by 3 · see citing works
Wang, J. Y. J., Minami, Y., & Zhu, J. (2008) · Springer eBooks · doi:10.1007/978-0-387-68744-5_4 · Cited by 3 · see citing works
The FABD domain is critical for the oncogenicity of BCR/ABL in chronic myeloid leukaemia
Zheng, R., Wei, W., Liu, S., Zeng, D., Yang, Z., Tang, J., Tan, J., Huang, Z., & Gao, M. (2024) · Cell Communication and Signaling · doi:10.1186/s12964-024-01694-8 · Cited by 2 · see citing works
Gurianov, D. S., Antonenko, S. V., & Телегеев, Г. Д. (2021) · Experimental Oncology · doi:10.32471/exp-oncology.2312-8852.vol-43-no-1.15811 · Cited by 2 · see citing works
Massimino, M., Stella, S., Romano, C., Buffa, P., Tirrò, E., Drago, M., Manzella, L., Tomarchio, C., Vitale, S. R., Raimondo, F. D., et al. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26146591 · Cited by 2 · see citing works
Imatinib Mesylate (Gleevec®) and the Emergence of Chemotherapeuticss Drug-Resistant Mutations
Denis, G. V. (2007) · Humana Press eBooks · doi:10.1007/978-1-59745-337-0_22 · Cited by 2 · see citing works
Casolari, D. A., & Melo, J. V. (2015) · Springer eBooks · doi:10.1007/978-3-319-19983-2_7 · Cited by 2 · see citing works
Wolff, L., Ackerman, S. J., & Nucifora, G. (2005) · Experimental Hematology · doi:10.1016/j.exphem.2005.09.011 · Cited by 1 · see citing works
Molecular Pathogenesis of BCR‐ABL in Chronic Myeloid Leukemia
Padron, E., Hazlehurst, L., & Pinilla-Ibarz, J. A. (2011) · Wiley eBooks · doi:10.1002/9781444394016.ch4 · Cited by 1 · see citing works
The DNA Replication Initiation Machinery as a Target for Cancer Diagnosis and Therapy
Wollenschlaeger, A. (2011) · EUR Research Repository (Erasmus University Rotterdam) · Cited by 1 · see citing works
Mughal, T. I., & Goldman, J. M. (2006) · Clinical Leukemia · doi:10.3816/clk.2006.n.015 · Cited by 1 · see citing works
Getting to the root of the stem cell in mutated chronic myeloid leukemia
Larson, S. M., & Godley, L. A. (2010) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.3109/10428194.2010.531802 · Cited by 1 · see citing works
Modeling Human Philadelphia Chromosome-Positive Leukemia in Mice
Li, S. (2008) · Springer eBooks · doi:10.1007/978-0-387-69132-9_7
- Authors
- Dierov, J., Dierova, R., & Carroll, M.
- Affiliations
- University of Pennsylvania (US)
- Corresponding author
- Carroll, Martin
- ORCID
- Carroll, Martin
- Venue
- Cancer Cell
- Publisher
- Elsevier BV
- Published
- 2004-03
- Volume
- 5
- Issue
- 3
- Pages
- 275-285
- ISSN
- 1535-6108 (ISSN-L)
- OpenAlex
- W2035713316
- Cited by
- 117
- References
- 40
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 3 · 2023: 1 · 2022: 1 · 2021: 2 · 2020: 4 · 2018: 3 · 2017: 4 · 2016: 2 · 2015: 3 · 2014: 4 · 2013: 2 · 2012: 9
- FWCI
- 7.97
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cancer Cell (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Hematology › Chronic Myeloid Leukemia Treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
- Keywords
- BCR-ABL, chronic myeloid leukemia, nuclear translocation, ATR, S-phase checkpoint, DNA damage response, radioresistant DNA synthesis, etoposide, DNA double-strand breaks, blast crisis, tyrosine kinase
- MeSH terms
- Cell Nucleus, Cells, Cultured, Cytoplasm, DNA Damage, DNA Topoisomerases, Type II, DNA Repair, Enzyme Inhibitors, Etoposide, Humans, Signal Transduction, Leukemia, Myelogenous, Chronic, BCR-ABL Positive, Fusion Proteins, bcr-abl, S Phase, Protein Serine-Threonine Kinases, Cell Cycle Proteins, Protein Transport, Ataxia Telangiectasia Mutated Proteins
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